A dynamic formin-dependent deep F-actin network in axons

Journal of Cell Biology

Volumn 210, Issue 3, 2015, Pages 401-417

  Ganguly, Archan ^a   Tang, Yong ^a   Wang, Lina ^a   Ladt, Kelsey ^a,b   Loi, Jonathan ^a   Dargent, Bénédicte ^c   Leterrier, Christophe ^c   Roy, Subhojit ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of Mediterranée   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; F ACTIN; FORMIN PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ACTIN; ACTIN BINDING PROTEIN; ENHANCED GREEN FLUORESCENT PROTEIN; FETOPROTEIN; FORMIN 1; GREEN FLUORESCENT PROTEIN; NUCLEAR PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOSOME; MOLECULAR IMAGING; MOUSE; NERVE CELL MEMBRANE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN METABOLISM; SYNAPSE; SYNAPSE VESICLE; ANIMAL; ANTAGONISTS AND INHIBITORS; AXON; BIOSYNTHESIS; CELL MEMBRANE; GROWTH CONE; METABOLISM; MICROTUBULE; NERVE ENDING; PHYSIOLOGY;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ANIMALS; AXONS; CELL MEMBRANE; FETAL PROTEINS; GREEN FLUORESCENT PROTEINS; GROWTH CONES; MICE; MICROFILAMENT PROTEINS; MICROTUBULES; NUCLEAR PROTEINS; PRESYNAPTIC TERMINALS; SYNAPTIC VESICLES;

EID: 84938656289     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201506110     Document Type: Article

References (71)

1. Balaji, J., and T.A. Ryan. 2007. Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode. Proc. Natl. Acad. Sci. USA. 104:20576-20581. http://dx.doi.org/10.1073/pnas.0707574105.
2. Bearer, E.L., and T.S. Reese. 1999. Association of actin filaments with axonal microtubule tracts. J. Neurocytol. 28:85-98. http://dx.doi.org/10.1023/A:1007025421849.
3. Bernstein, B.W., M. DeWit, and J.R. Bamburg. 1998. Actin disassembles reversibly during electrically induced recycling of synaptic vesicles in cultured neurons. Brain Res. Mol. Brain Res. 53:236-250. http://dx.doi.org/10.1016/S0169-328X(97)00319-7.
4. Black, M.M., and R.J. Lasek. 1979. Axonal transport of actin: slow component b is the principal source of actin for the axon. Brain Res. 171:401-413. http://dx.doi.org/10.1016/0006-8993(79)91045-X.
5. Bridgman, P.C. 2009. Myosin motor proteins in the cell biology of axons and other neuronal compartments. Results Probl. Cell Differ. 48:91-105.
6. Bubb, M.R., A.M. Senderowicz, E.A. Sausville, K.L. Duncan, and E.D. Korn. 1994. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J. Biol. Chem. 269:14869-14871.
7. Burkel, B.M., G. von Dassow, and W.M. Bement. 2007. Versatile fluorescent probes for actin filaments based on the actin-binding domain of utrophin. Cell Motil. Cytoskeleton. 64:822-832. http://dx.doi.org/10.1002/cm.20226.
8. Chesarone, M.A., A.G. DuPage, and B.L. Goode. 2010. Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat. Rev. Mol. Cell Biol. 11:62-74. http://dx.doi.org/10.1038/nrm2816.
9. Chia, P.H., P. Li, and K. Shen. 2013. Cell biology in neuroscience: cellular and molecular mechanisms underlying presynapse formation. J. Cell Biol. 203:11-22. http://dx.doi.org/10.1083/jcb.201307020.
10. Chia, P.H., B. Chen, P. Li, M.K. Rosen, and K. Shen. 2014. Local F-actin network links synapse formation and axon branching. Cell. 156:208-220. http://dx.doi.org/10.1016/j.cell.2013.12.009.
11. Christensen, R., Z. Shao, and D.A. Colón-Ramos. 2013. The cell biology of synaptic specificity during development. Curr. Opin. Neurobiol. 23:1018-1026. http://dx.doi.org/10.1016/j.conb.2013.07.004.
12. Cingolani, L.A., and Y. Goda. 2008. Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 9:344-356. http://dx.doi.org/10.1038/nrn2373.
13. Cooper, J.A. 1987. Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105:1473-1478. http://dx.doi.org/10.1083/jcb.105.4.1473.
14. D'Este, E., D. Kamin, F. Göttfert, A. El-Hady, and S.W. Hell. 2015. STED nanoscopy reveals the ubiquity of subcortical cytoskeleton periodicity in living neurons. Cell Reports. 10:1246-1251. http://dx.doi.org/10.1016/j.celrep.2015.02.007.
15. Dent, E.W., S.L. Gupton, and F.B. Gertler. 2011. The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb. Perspect. Biol. 3:a001800. http://dx.doi.org/10.1101/cshperspect.a001800.
16. El Meskini, R., L.B. Cline, B.A. Eipper, and G.V. Ronnett. 2005. The developmentally regulated expression of Menkes protein ATP7A suggests a role in axon extension and synaptogenesis. Dev. Neurosci. 27:333-348. http://dx.doi.org/10.1159/000086713.
17. Fath, K.R., and R.J. Lasek. 1988. Two classes of actin microfilaments are associated with the inner cytoskeleton of axons. J. Cell Biol. 107:613-621. http://dx.doi.org/10.1083/jcb.107.2.613.
18. Field, C.M., and P. Lénárt. 2011. Bulk cytoplasmic actin and its functions in meiosis and mitosis. Curr. Biol. 21:R825-R830. http://dx.doi.org/10.1016/j.cub.2011.07.043.
19. Flynn, K.C., C.W. Pak, A.E. Shaw, F. Bradke, and J.R. Bamburg. 2009. Growth cone-like waves transport actin and promote axonogenesis and neurite branching. Dev. Neurobiol. 69:761-779. http://dx.doi.org/10.1002/dneu.20734.
20. Galbraith, J.A., and P.E. Gallant. 2000. Axonal transport of tubulin and actin. J. Neurocytol. 29:889-911. http://dx.doi.org/10.1023/A:1010903710160.
21. Ganguly, A., and S. Roy. 2014. Using photoactivatable GFP to track axonal transport kinetics. Methods Mol. Biol. 1148:203-215. http://dx.doi.org/10.1007/978-1-4939-0470-9_13.
22. Gomez, T.M., and P.C. Letourneau. 2014. Actin dynamics in growth cone motility and navigation. J. Neurochem. 129:221-234. http://dx.doi.org/10.1111/jnc.12506.
23. Goode, B.L., A.A. Rodal, G. Barnes, and D.G. Drubin. 2001. Activation of the Arp2/3 complex by the actin filament binding protein Abp1p. J. Cell Biol. 153:627-634. http://dx.doi.org/10.1083/jcb.153.3.627.
24. Gotow, T., K. Miyaguchi, and P.H. Hashimoto. 1991. Cytoplasmic architecture of the axon terminal: filamentous strands specifically associated with synaptic vesicles. Neuroscience. 40:587-598. http://dx.doi.org/10.1016/0306-4522(91)90143-C.
25. Higashida, C., T. Miyoshi, A. Fujita, F. Oceguera-Yanez, J. Monypenny, Y. Andou, S. Narumiya, and N. Watanabe. 2004. Actin polymerization-driven molecular movement of mDia1 in living cells. Science. 303:2007-2010. http://dx.doi.org/10.1126/science.1093923.
26. Hirokawa, N. 1982. Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method. J. Cell Biol. 94:129-142. http://dx.doi.org/10.1083/jcb.94.1.129.
27. Hirokawa, N., K. Sobue, K. Kanda, A. Harada, and H. Yorifuji. 1989. The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. J. Cell Biol. 108:111-126. http://dx.doi.org/10.1083/jcb.108.1.111.
28. Huang, B., W. Wang, M. Bates, and X. Zhuang. 2008. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science. 319:810-813. http://dx.doi.org/10.1126/science.1153529.
29. Jareb, M., and G. Banker. 1997. Inhibition of axonal growth by brefeldin A in hippocampal neurons in culture. J. Neurosci. 17:8955-8963.
30. Kaech, S., C.F. Huang, and G. Banker. 2012. Short-term high-resolution imaging of developing hippocampal neurons in culture. Cold Spring Harb Protoc. 2012:340-343
31. Ladt, K., A. Ganguly, and S. Roy. 2015. Axonal actin in action: imaging actin dynamics in neurons. Methods Cell Biol. http://dx.doi.org/10.1016/bs.mcb.2015.07.003.
32. Landis, D.M., A.K. Hall, L.A. Weinstein, and T.S. Reese. 1988. The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron 1: 201-209. http://dx.doi.org/10.1016/0896-6273(88)90140-7
33. Letourneau, P.C. 2009. Actin in axons: stable scaffolds and dynamic filaments. Results Probl. Cell Differ. 48:65-90.
34. Loudon, R.P., L.D. Silver, H.F. Yee Jr., and G. Gallo. 2006. RhoA-kinase and myosin II are required for the maintenance of growth cone polarity and guidance by nerve growth factor. J. Neurobiol. 66:847-867. http://dx.doi.org/10.1002/neu.20258.
35. Lukinavicius, G., L. Reymond, E. D'Este, A. Masharina, F. Göttfert, H. Ta, A. Güther, M. Fournier, S. Rizzo, H. Waldmann, et al. 2014. Fluorogenic probes for live-cell imaging of the cytoskeleton. Nat. Methods. 11:731-733. http://dx.doi.org/10.1038/nmeth.2972.
36. Melom, J.E., Y. Akbergenova, J.P. Gavornik, and J.T. Littleton. 2013. Spontaneous and evoked release are independently regulated at individual active zones. J. Neurosci. 33:17253-17263. http://dx.doi.org/10.1523/JNEUROSCI.3334-13.2013.
37. Michelot, A., and D.G. Drubin. 2011. Building distinct actin filament networks in a common cytoplasm. Curr. Biol. 21:R560-R569. http://dx.doi.org/10.1016/j.cub.2011.06.019.
38. Morales, M., M.A. Colicos, and Y. Goda. 2000. Actin-dependent regulation of neurotransmitter release at central synapses. Neuron. 27:539-550. http://dx.doi.org/10.1016/S0896-6273(00)00064-7.
39. Morton, W.M., K.R. Ayscough, and P.J. McLaughlin. 2000. Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat. Cell Biol. 2:376-378. http://dx.doi.org/10.1038/35014075.
40. Nelson, J.C., A.K. Stavoe, and D.A. Colón-Ramos. 2013. The actin cytoskeleton in presynaptic assembly. Cell Adhes. Migr. 7:379-387. http://dx.doi.org/10.4161/cam.24803.
41. Nolen, B.J., N. Tomasevic, A. Russell, D.W. Pierce, Z. Jia, C.D. McCormick, J. Hartman, R. Sakowicz, and T.D. Pollard. 2009. Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature. 460:1031-1034. http://dx.doi.org/10.1038/nature08231.
42. Okabe, S., and N. Hirokawa. 1990. Turnover of fluorescently labelled tubulin and actin in the axon. Nature. 343:479-482. http://dx.doi.org/10.1038/343479a0.
43. Ovesnỳ, M., P. Krížek, J. Borkovec, Z. Svindrych, and G.M. Hagen. 2014. ThunderSTORM: a comprehensive ImageJ plug-in for PALM and STORM data analysis and super-resolution imaging. Bioinformatics. 30:2389-2390. http://dx.doi.org/10.1093/bioinformatics/btu202.
44. Pfender, S., V. Kuznetsov, S. Pleiser, E. Kerkhoff, and M. Schuh. 2011. Spiretype actin nucleators cooperate with Formin-2 to drive asymmetric oocyte division. Curr. Biol. 21:955-960. http://dx.doi.org/10.1016/j.cub.2011.04.029.
45. Prekeris, R., D.L. Foletti, and R.H. Scheller. 1999. Dynamics of tubulovesicular recycling endosomes in hippocampal neurons. J. Neurosci. 19:10324-10337.
46. Riedl, J., A.H. Crevenna, K. Kessenbrock, J.H. Yu, D. Neukirchen, M. Bista, F. Bradke, D. Jenne, T.A. Holak, Z. Werb, et al. 2008. Lifeact: a versatile marker to visualize F-actin. Nat. Methods. 5:605-607. http://dx.doi.org/10.1038/nmeth.1220.
47. Rizvi, S.A., E.M. Neidt, J. Cui, Z. Feiger, C.T. Skau, M.L. Gardel, S.A. Kozmin, and D.R. Kovar. 2009. Identification and characterization of a small molecule inhibitor of formin-mediated actin assembly. Chem. Biol. 16:1158-1168. http://dx.doi.org/10.1016/j.chembiol.2009.10.006.
48. Roy, S., G. Yang, Y. Tang, and D.A. Scott. 2012. A simple photoactivation and image analysis module for visualizing and analyzing axonal transport with high temporal resolution. Nat. Protoc. 7:62-68. http://dx.doi.org/10.1038/nprot.2011.428.
49. Ruthel, G., and G. Banker. 1998. Actin-dependent anterograde movement of growth-cone-like structures along growing hippocampal axons: a novel form of axonal transport? Cell Motil. Cytoskeleton. 40:160-173. http://dx.doi.org/10.1002/(SICI)1097-0169(1998)40:2<160::AID-CM5>3.0.CO;2-J.
50. Ryan, T.A. 1999. Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J. Neurosci. 19:1317-1323.
51. Saheki, Y., and P. De Camilli. 2012. Synaptic vesicle endocytosis. Cold Spring Harb. Perspect. Biol. 4:a005645. http://dx.doi.org/10.1101/cshperspect.a005645.
52. Sankaranarayanan, S., P.P. Atluri, and T.A. Ryan. 2003. Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat. Neurosci. 6:127-135. http://dx.doi.org/10.1038/nn1002.
53. Schafer, D.P., S. Jha, F. Liu, T. Akella, L.D. McCullough, and M.N. Rasband. 2009. Disruption of the axon initial segment cytoskeleton is a new mechanism for neuronal injury. J. Neurosci. 29:13242-13254. http://dx.doi.org/10.1523/JNEUROSCI.3376-09.2009.
54. Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, et al. 2012. Fiji: an opensource platform for biological-image analysis. Nat. Methods. 9:676-682. http://dx.doi.org/10.1038/nmeth.2019.
55. Schnapp, B.J., and T.S. Reese. 1982. Cytoplasmic structure in rapid-frozen axons. J. Cell Biol. 94:667-669. http://dx.doi.org/10.1083/jcb.94.3.667.
56. Schuh, M. 2011. An actin-dependent mechanism for long-range vesicle transport. Nat. Cell Biol. 13:1431-1436. http://dx.doi.org/10.1038/ncb2353.
57. Scott, D., and S. Roy. 2012. a-Synuclein inhibits intersynaptic vesicle mobility and maintains recycling-pool homeostasis. J. Neurosci. 32:10129-10135. http://dx.doi.org/10.1523/JNEUROSCI.0535-12.2012.
58. Scott, D.A., U. Das, Y. Tang, and S. Roy. 2011. Mechanistic logic underlying the axonal transport of cytosolic proteins. Neuron. 70:441-454. http://dx.doi.org/10.1016/j.neuron.2011.03.022.
59. Shupliakov, O., O. Bloom, J.S. Gustafsson, O. Kjaerulff, P. Low, N. Tomilin, V.A. Pieribone, P. Greengard, and L. Brodin. 2002. Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc. Natl. Acad. Sci. USA. 99:14476-14481. http://dx.doi.org/10.1073/pnas.212381799.
60. Tang, Y., D.A. Scott, U. Das, S.D. Edland, K. Radomski, E.H. Koo, and S. Roy. 2012. Early and selective impairments in axonal transport kinetics of synaptic cargoes induced by soluble amyloid ß-protein oligomers. Traffic. 13:681-693. http://dx.doi.org/10.1111/j.1600-0854.2012.01340.x.
61. Tang, Y., D. Scott, U. Das, D. Gitler, A. Ganguly, and S. Roy. 2013. Fast vesicle transport is required for the slow axonal transport of synapsin. J. Neurosci. 33:15362-15375. http://dx.doi.org/10.1523/JNEUROSCI.1148-13.2013.
62. Tilney, L.G., and D.A. Portnoy. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1597-1608. http://dx.doi.org/10.1083/jcb.109.4.1597.
63. Vidali, L., P.A. van Gisbergen, C. Guérin, P. Franco, M. Li, G.M. Burkart, R.C. Augustine, L. Blanchoin, and M. Bezanilla. 2009. Rapid formin-mediated actin-filament elongation is essential for polarized plant cell growth. Proc. Natl. Acad. Sci. USA. 106:13341-13346. http://dx.doi.org/10.1073/pnas.0901170106.
64. Voglmaier, S.M., K. Kam, H. Yang, D.L. Fortin, Z. Hua, R.A. Nicoll, and R.H. Edwards. 2006. Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron. 51:71-84. http://dx.doi.org/10.1016/j.neuron.2006.05.027.
65. Waites, C.L., S.A. Leal-Ortiz, T.F. Andlauer, S.J. Sigrist, and C.C. Garner. 2011. Piccolo regulates the dynamic assembly of presynaptic F-actin. J. Neurosci. 31:14250-14263. http://dx.doi.org/10.1523/JNEUROSCI.1835-11.2011.
66. Wang, X.H., J.Q. Zheng, and M.M. Poo. 1996. Effects of cytochalasin treatment on short-term synaptic plasticity at developing neuromuscular junctions in frogs. J. Physiol. 491:187-195. http://dx.doi.org/10.1113/jphysiol.1996.sp021206.
67. Wang, L., U. Das, D.A. Scott, Y. Tang, P.J. McLean, and S. Roy. 2014. a-synuclein multimers cluster synaptic vesicles and attenuate recycling. Curr. Biol. 24:2319-2326. http://dx.doi.org/10.1016/j.cub.2014.08.027.
68. Watanabe, S., T. Trimbuch, M. Camacho-Pérez, B.R. Rost, B. Brokowski, B. Söhl-Kielczynski, A. Felies, M.W. Davis, C. Rosenmund, and E.M. Jorgensen. 2014. Clathrin regenerates synaptic vesicles from endosomes. Nature. 515:228-233. http://dx.doi.org/10.1038/nature13846.
69. Willard, M., M. Wiseman, J. Levine, and P. Skene. 1979. Axonal transport of actin in rabbit retinal ganglion cells. J. Cell Biol. 81:581-591. http://dx.doi.org/10.1083/jcb.81.3.581.
70. Xu, K., G. Zhong, and X. Zhuang. 2013. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science. 339:452-456. http://dx.doi.org/10.1126/science.1232251.
71. Zhong, G., J. He, R. Zhou, D. Lorenzo, H.P. Babcock, V. Bennett, and X. Zhuang. 2014. Developmental mechanism of the periodic membrane skeleton in axons. eLife. 3. http://dx.doi.org/10.7554/eLife.04581.